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Absence of adrenergic red cell pH and oxygen content regulation in American eel (Anguilla rostrata) during hypercapnic acidosis in vivo and in vitro

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Summary

American eels (Anguilla rostrata) were exposed to acute (30 min) external hypercapnia (1% CO2 or 5% CO2 in air) in order to assess the involvement of circulating catecholamines in regulating red blood cell (RBC) pH and oxygen content during whole blood acidosis. Plasma adrenaline levels increased approximately 5-fold during severe hypercapnia yet absolute levels remained below 1.0 nM; plasma noradrenaline levels were unchanged. Both RBC pH and oxygen bound to haemoglobin ([O2]/[Hb]) conformed to in vitro relationships with whole blood pH (pHe) indicating absence of regulation during hypercapnia in vivo. Pre-treatment of eels with α- or β-adrenoceptor antagonists, phentolamine or propranolol was without effect on RBC pH or [O2]/[Hb] during hypercapnia. Further, intra-arterial injection of adrenaline (final plasma concentration=134 nM) or noradrenaline (final plasma concentration = 34 nM) into hypercapnic eels 5 min prior to blood sampling did not modify any measured blood variable RBC nucleoside triphosphate (NTP) levels, RBC pH and [O2]/[Hb]. In vitro, the application of adrenaline or noradrenaline to eel RBC's during graded normoxic hypercapnia or hypoxic hypercapnia (noradrenaline only) did not affect RBC pH significantly. RBC NTP levels were depressed by noradrenaline in vitro but only during hypoxic hypercapnia.

The results demonstrate adrenergic insensitivity of eel RBC's in vivo even under conditions (acidosis, hypoxemia) known to enhance catecholamine-mediated RBC responses in other species. We conclude that the American eel has no capacity to regulate RBC pH during hypercapnia and consequently [O2]/[Hb] is reduced in accordance with the in vitro Root effect.

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References

  • Baroin A, Garcia-Romeu F, Lamarre T, Motais R (1984) A transient sodium/hydrogen exchange system induced by catecholamines in erythrocytes of rainbow trout,Salmo gairdneri. J Physiol Lond 356:21–32

    Google Scholar 

  • Bennett MB, Rankin JC (1985) Identification of beta-adrenergic receptors in teleost red blood cells. Comp Biochem Physiol 81C:411–414

    Google Scholar 

  • Borgese F, Garcia-Romeu F, Motais R (1987) Control of cell volume and ion transport by beta-adrenergic catecholamines in erythrocytes of rainbow trout,Salmo gairdneri. J Physiol 382:123–144

    Google Scholar 

  • Boutilier RG, Heming TA, Iwama GK (1984) Physico-chemical parameters for use in fish respiratory physiology. In Hoar WS, Randall DJ (eds)Fish Physiology, Vol. XA. Academic Press, New York, pp 401–430

    Google Scholar 

  • Boutilier RG, Iwama GK, Randall DJ (1986) Acute extracellular acidosis promotes catecholamine release in rainbow trout (Salmo gairdneri): interactions between red cell pH and O2−Hb carrying capacity. J Exp Biol 123:145–157

    Google Scholar 

  • Boutilier RG, Dobson G, Hoeger U, Randall DJ (1988) Acute exposure to graded levels of hypoxia in rainbow trout (Salmo gairdneri): metabolic and respiratory adaptations. Respir Physiol 71:69–82

    Google Scholar 

  • Cossins AR, Richardson PA (1985) Adrenalin-induced Na+/H+ exchange in trout erythrocytes and its effects upon oxygen carrying capacity. J Exp Biol 118:229–246

    Google Scholar 

  • Davie PS (1981) Vascular resistance responses of an eel tail preparation: alpha constriction and beta dilation. J Exp Biol 90:65–84

    Google Scholar 

  • Epple A, Vogel WH, Nibbio B (1982) Catecholamines in head and body of eels and rats. Comp Biochem Physiol 71C:115–118

    Google Scholar 

  • Epple A, Nibbio B (1985) Catecholaminotropic effects of catecholamines in a teleost fish,Anguilla rostrata. J Comp Physiol B 155:285–290

    Google Scholar 

  • Fievet B, Motais R, Thomas S (1987) Role of adrenergic-dependent H+ release from red cells in acidosis induced by hypoxia in trout. Amer J Physiol 252:R269-R275

    Google Scholar 

  • Forster ME (1976) Effects of catecholamines on the heart and on branchial and peripheral resistances of the eel.Anguilla anguilla (L.). Comp Biochem Physiol 55:27–32

    Google Scholar 

  • Fuchs DA, Albers C (1988) Effect of adrenaline and blood gas conditions on red cell volume and intra-erythrocyte electrolytes in the carp,Cyprinus carpio. J Exp Biol 137:457–477

    Google Scholar 

  • Hyde DA, Moon TW, Perry SF (1987) Physiological consequences of prolonged aerial exposure in the American eel,Anguilla rostrata: Blood respiratory and acid-base status. J Comp Physiol B 157:635–642

    Google Scholar 

  • Hyde DA, Perry SF (in press) Differential approaches to blood acid-base regulation during exposure to prolonged hypercapnia in two freshwater teleosts: the rainbow trout (Salmo gairdneri) and the American eel (Anguilla rostrata). Physiol Zool

  • Jensen FB, Weber RE (1982) Respiratory properties of tench blood and haemoglobin. Adaptation to hypoxic-hypercapnic water. Molec Physiol 2:235–245

    Google Scholar 

  • Jensen FB, Weber RE (1985) Kinetics of the acclimational responses of tench to combined hypoxia and hypercapnia. II. Extra- and intracellular acid-base status in the blood. J Comp Physiol B 156:205–211

    Google Scholar 

  • Jensen FB (1987) Influences of exercise-stress and adrenaline upon intra- and extracellular acid-base status, electrolyte composition and respiratory properties of blood in tench (Tinca tinca) at different seasons. J Comp Physiol B 157:51–60

    Google Scholar 

  • LeBras YM (1982) Effects of anaesthesia and surgery on levels of adrenaline and noradrenaline in blood plasma of the eel (Anguilla anguilla L.). Comp Biochem Physiol 72C:141–144

    Google Scholar 

  • Lykkeboe G, Weber RE (1978) Changes in the respiratory properties of the blood of the carp,Cyprinus carpio, induced by diurnal variation in ambient oxygen tension. J Comp Physiol B 128:117–125

    Google Scholar 

  • Milligan CL, Wood CM (1986) Intracellular and extracellular acid-base status and H+ exchange with the environment after exhaustive exercise in the rainbow trout. J Exp Biol 123:93–121

    Google Scholar 

  • Milligan CL, Wood CM (1987) Regulation of blood oxygen transport and red cell pH after exhaustive activity in rainbow trout (Salmo gairdneri) and starry flounder (Platichthys stellatus). J Exp Biol 133:263–282

    Google Scholar 

  • Motais R, Garcia-Romeu F, Borgese F (1987) The control of Na+/H+ exchange by molecular oxygen in trout erythrocytes: A possible role of hemoglobin as a transducer. J Gen Physiol 90:197–207

    Google Scholar 

  • Nikinmaa M (1982) Effects of adrenaline on red cell volume and concentration gradient of protons across the red cell membrane in the rainbow trout,Salmo gairdneri. Molec Physiol 2:287–297

    Google Scholar 

  • Nikinmaa M, Cech JJ, McEnroe M (1984) Blood oxygen transport in striped bass (Morone saxatilis): role of beta-adrenergic responses. J Comp Physiol B 154:365–369

    Google Scholar 

  • Nikinmaa M (1986) Control of red cell pH in teleost fishes. Ann Zool Fennici 23:223–235

    Google Scholar 

  • Nikinmaa M, Steffensen JF, Tufts BL, Randall DJ (1987a) Control of red cell volume and pH in trout: effects of isoproterenol, transport inhibitors and extracellular pH in bicarbonate/carbon dioxide-buffered media. J Exp Zool 242:273–281

    Google Scholar 

  • Nikinmaa M, Cech JJ Jr, Ryhänen E-L, Salama A (1987b) Red cell function of carp (Cyprinus carpio) in acute hypoxia. Exp Biol 47:53–58

    Google Scholar 

  • Perry SF, Malone S, Ewing D (1987) Hypercapnic acidosis in the rainbow trout,Salmo gairdneri. I. Branchial ionic fluxes and blood acid-base status. Can J Zool 65:888–895

    Google Scholar 

  • Perry SF, Vermette MG (1987) The effects of continuous epinephrine infusion on the physiology of the rainbow trout,Salmo gairdneri. I. Blood respiratory, ionic and acid-base status. J Exp Biol 128:235–253

    Google Scholar 

  • Perry SF, Kinkead R, Gallaugher P, Randall DJ (in press) Evidence that hypoxemia promotes catecholamine release during hypercapnic acidosis in rainbow trout (Salmo gairdneri). Respir Physiol

  • Perry SF, Kinkead R (in press) The role of catecholamines in regulating arterial oxygen content during acute hypercapnic acidosis in rainbow trout (Salmo gairdneri). Respir Physiol

  • Perry SF, Wood CM (in press) Control and coordination of gas transfer in fishes. Can J Zool

  • Peyraud-Waitznegger M (1979) Simultaneous modifications of ventilation and arterialPO2 by catecholamines in the eel,Anguilla anguilla L.: participation of α and β effects. J Comp Physiol 129:343–354

    Google Scholar 

  • Primmett DRN, Randall DJ, Mazeaud MM, Boutilier RG (1986) The role of catecholamines in erythrocyte pH regulation and oxygen transport in rainbow trout during exercise. J Exp Biol 122:139–148

    Google Scholar 

  • Soivio A, Nikinmaa M, Westman K (1980) The blood oxygen binding properties of hypoxicSalmo gairdneri. J Comp Physiol 136:83–87

    Google Scholar 

  • Tetens V, Lykkeboe G (1985) Acute exposure of rainbow trout to mild and deep hypoxia: O2 affinity and O2 capacitance of arterial blood. Respir Physiol 61:221–235

    Google Scholar 

  • Tetens V, Lykkeboe G, Christensen NJ (1988) Potency of adrenaline and noradrenaline for beta-adrenergic proton extrusion from red cells of rainbow trout,Salmo gairdneri. J Exp Biol 134:267–280

    Google Scholar 

  • Tucker VA (1967) A method for oxygen content and dissociation curves on microliter blood samples. J Appl Physiol 23:407–410

    Google Scholar 

  • Vermette MG, Perry SF (1988a) Adrenergic involvement in blood oxygen tranport and acid-base balance during hypercapnic acidosis in the rainbow trout,Salmo gairdneri. J Comp Physiol B 158:107–115

    Google Scholar 

  • Vermette MG, Perry SF (1988b) Effects of prolonged epinephrine infusion on blood respiratory and acid-base states in the rainbow trout: alpha and beta effects. Fish Physiol Biochem 4:189–202

    Google Scholar 

  • Walker RL, Wilkes PRH, Wood CM (1989) The effects of hypersaline exposure on the blood oxygen affinity of the fresh-water teleostCatastomus commersoni. J Exp Biol 142:125–142

    Google Scholar 

  • Wood SC, Johansen K, Weber R (1975) Effects of ambientPO2 on hemoglobin-oxygen affinity and red cell ATP concentrations in a benthic fish,Pleuronectes platessa. Respir Physiol 25:259–267

    Google Scholar 

  • Woodward JJ (1982) Plasma catecholamines in resting rainbow trout,Salmo gairdneri Richardson, by high pressure liquid chromatography. J Fish Biol 21:429–432

    Google Scholar 

  • Wolf K (1963) Physiological salines for freshwater teleosts. Prog Fish Cult 25:135–140

    Google Scholar 

  • Zeidler R, Kim HD (1977) Preferential haemolysis of postnatal calf red cells induced by internal alkalinization. J Gen Physiol 70:385–401

    Google Scholar 

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Hyde, D.A., Perry, S.F. Absence of adrenergic red cell pH and oxygen content regulation in American eel (Anguilla rostrata) during hypercapnic acidosis in vivo and in vitro. J Comp Physiol B 159, 687–693 (1990). https://doi.org/10.1007/BF00691714

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